Unidirectionality of charge separation in reaction centers of photosynthetic bacteria

Abstract Time-resolved spectroscopy in conjunction with X-ray structural data for reaction centers of Rhodopseudomonas viridis and Rhodobacter sphaeroides reveal a branching ratio a > 5 for the primary electron-transfer rates, favouring one of the two, almost symmetrical pigment/protein branches, L and M. In this paper we explore the origins of this unidirectionality of electron transfer between the excited singlet state of the bacteriochlorophyll dimer ( 1 P∗) and the bacteriopheophytin (H) along the L protein subunit. Nonadiabatic electron-transfer theory is applied to analyze the asymmetry of the electron-transfer rates, k L and k M across the L and M branches. The asymmetry originates from the cumulative contributions of the nuclear Franck-Condon factor and the electronic coupling, both of which enhance the electron transfer rate across the L branch. The nuclear Frank-Condon factors are modified by the energy difference ΔE LM between the states P + H − L and P + H − M , which is induced by the electrostatic interactions of these ion-pair states with the protein polar groups, as well as by asymmetric Coulomb and medium polarization interactions. The computation results in ΔE LM = −(0.09 ± 0.04) eV, which yields a nuclear enhancement contribution at 300 K of 1.5 (+0.8, −0.3) to k L k M and therefore is insufficient to explain alone the observed asymmetry in reaction centers of Rps. viridis . Another contribution to the unidirectionality originates from electronic superexchange coupling for 1 P∗-B-H via the virtual states of the accessory bacteriochlorophyll (B). The ratio of the intermolecular 1 P∗-B L and 1 P∗-B M electronic interaction terms was evaluated utilizing the tight-binding approximation with SCF-MO wavefunctions, together with the structural data for the prosthetic groups and for the polar amino acid side chains of the protein in reaction centers of Rps. viridis . The contribution to the enhancement of k L k M by the electronic superexchange is approx. 8 ± 4. This asymmetry was traced to the combination of an excess negative charge density on the M-dimer component P M , together with structural asymmetry, which enhances the P M -B L electronic overlap. Consequently, the 1 P∗-B L -H L superexchange is favoured over the 1 P∗-B M -H M interaction. The combined effects of asymmetric nuclear Franck-Condon factors and electronic couplings yield a branching ratio of the electron-transfer rates along the two pigment branches in reaction centers of Rps. viridis of an approx. 12 (−7, +15). This is sufficiently large to explain the experimentally observed unidirectionality.

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